Erythroid Differentiation Sensitizes K562 Leukemia Cells to TRAIL-Induced Apoptosis by Downregulation of c-FLIP

REFERENCES

• Altucci, L., A. Rossin, W. Raffelsberger, A. Reitmair, C. Chomienne, and H. Gronemeyer. 2001. Retinoic acid-induced apoptosis in leukemia cells is mediated by paracrine action of tumor-selective death ligand TRAIL. Nat. Med. 7: 680–686.
   PubMed Web of Science ®Google Scholar
• Andersson, L. C., M. Jokinen, and C. G. Gahmberg. 1979. Induction of erythroid differentiation in the human leukaemia cell line K562. Nature 278: 364–365.
   PubMedGoogle Scholar
• Aoudjit, F., and K. Vuori. 2001. Matrix attachment regulates Fas-induced apoptosis in endothelial cells: a role for c-Flip and implications for anoikis. J. Cell Biol. 152: 633–643.
   PubMed Web of Science ®Google Scholar
• Ashkenazi, A., R. C. Pai, S. Fong, S. Leung, D. A. Lawrence, S. A. Marsters, C. Blackie, L. Chang, A. E. McMurtrey, A. Hebert, L. DeForge, I. L. Koumenis, D. Lewis, L. Harris, J. Bussiere, H. Koeppen, Z. Shahrokh, and R. H. Schwall. 1999. Safety and antitumor activity of recombinant soluble Apo2 ligand. J. Clin. Investig. 104: 155–162.
   PubMed Web of Science ®Google Scholar
• Benito, A., M. Silva, D. Grillot, G. Nunez, and J. L. Fernandez-Luna. 1996. Apoptosis induced by erythroid differentiation of human leukemia cell lines is inhibited by Bcl-XL. Blood 87: 3837–3843.
   PubMed Web of Science ®Google Scholar
• Bodmer, J. L., N. Holler, S. Reynard, P. Vinciguerra, P. Schneider, P. Juo, J. Blenis, and J. Tschopp. 2000. TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat. Cell Biol. 2: 241–243.
   PubMed Web of Science ®Google Scholar
• Chang, D. W., Z. Xing, Y. Pan, A. Algeciras-Schimnich, B. C. Barnhart, S. Yaish-Ohad, M. E. Peter, and X. Yang. 2002. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J. 21: 3704–3714.
   PubMed Web of Science ®Google Scholar
• Chinnaiyan, A. M., U. Prasad, S. Shankar, D. A. Hamstra, M. Shanaiah, T. L. Chenevert, B. D. Ross, and A Rehemtulla. 2000. Combined effect of tumor necrosis factor-related apoptosis-inducing ligand and ionizing radiation in breast cancer therapy. Proc. Natl. Acad. Sci. USA 97: 1754–1759.
   PubMed Web of Science ®Google Scholar
• Collins, S. J., F. W. Ruscetti, R. E. Gallagher, and R. C. Gallo. 1978. Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc. Natl. Acad. Sci. USA 75: 2458–2462.
   PubMed Web of Science ®Google Scholar
• Cretney, E., K. Takeda, H. Yagita, M. Glaccum, J. J. Peschon, and M. J. Smyth. 2002. Increased susceptibility to tumor initiation and metastasis in TNF-related apoptosis-inducing ligand-deficient mice. J. Immunol. 168: 1356–1361.
   PubMed Web of Science ®Google Scholar
• De Maria, R., U. Testa, L. Luchetti, A. Zeuner, G. Stassi, E. Pelosi, R. Riccioni, N. Felli, P. Samoggia, and C. Peschle. 1999. Apoptotic role of Fas/Fas ligand system in the regulation of erythropoiesis. Blood 93: 796–803.
   PubMed Web of Science ®Google Scholar
• De Maria, R., A. Zeuner, A. Eramo, C. Domenichelli, D. Bonci, F. Grignani, S. M. Srinivasula, E. S. Alnemri, U. Testa, and C. Peschle. 1999. Negative regulation of erythropoiesis by caspase-mediated cleavage of GATA-1. Nature 401: 489–493.
   PubMed Web of Science ®Google Scholar
• Di Pietro, R., P. Secchiero, R. Rana, D. Gibellini, G. Visani, K. Bemis, L. Zamai, S. Miscia, and G. Zauli. 2001. Ionizing radiation sensitizes erythroleukemic cells but not normal erythroblasts to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated cytotoxicity by selective up-regulation of TRAIL-R1. Blood 97: 2596–2603.
   PubMed Web of Science ®Google Scholar
• Djerbi, M., V. Screpanti, A. I. Catrina, B. Bogen, P. Biberfeld, and A. Grandien. 1999. The inhibitor of death receptor signaling, FLICE-inhibitory protein defines a new class of tumor progression factors. J. Exp. Med. 190: 1025–1032.
   PubMed Web of Science ®Google Scholar
• Fukazawa, T., T. Fujiwara, F. Uno, F. Teraishi, Y. Kadowaki, T. Itoshima, Y. Takata, S. Kagawa, J. A. Roth, J. Tschopp, and N. Tanaka. 2001. Accelerated degradation of cellular FLIP protein through the ubiquitin-proteasome pathway in p53-mediated apoptosis of human cancer cells. Oncogene 20: 5225–5231.
   PubMed Web of Science ®Google Scholar
• Gibson, S. B., R. Oyer, A. C. Spalding, S. M. Anderson, and G. L. Johnson. 2000. Increased expression of death receptors 4 and 5 synergizes the apoptosis response to combined treatment with etoposide and TRAIL. Mol. Cell. Biol. 20: 205–212.
   PubMed Web of Science ®Google Scholar
• Gliniak, B., and T. Le. 1999. Tumor necrosis factor-related apoptosis-inducing ligand's antitumor activity in vivo is enhanced by the chemotherapeutic agent CPT-11. Cancer Res. 59: 6153–6158.
   PubMed Web of Science ®Google Scholar
• Goltsev, Y. V., A. V. Kovalenko, E. Arnold, E. E. Varfolomeev, V. M. Brodianskii, and D. Wallach. 1997. CASH, a novel caspase homologue with death effector domains. J. Biol. Chem. 272: 19641–19644.
   PubMed Web of Science ®Google Scholar
• Han, D. K. M., P. M. Chaudhary, M. E. Wright, C. Friedman, B. J. Trask, R. T. Riedel, D. G. Baskin, S. M. Schwartz, and L. Hood. 1997. MRIT, a novel death-effector domain-containing protein, interacts with caspases and BclX(L) and initiates cell death. Proc. Natl. Acad. Sci. USA 94: 11333–11338.
   PubMed Web of Science ®Google Scholar
• Hernandez, A., R. Thomas, F. Smith, J. Sandberg, S. Kim, D. H. Chung, and B. M. Evers. 2001. Butyrate sensitizes human colon cancer cells to TRAIL-mediated apoptosis. Surgery 130: 265–272.
   PubMedGoogle Scholar
• Holmstrüm, T. H., S. C. Chow, I. Elo, E. T. Coffey, S. Orrenius, L. Sistonen, and J. E. Eriksson. 1998. Suppression of Fas/APO-1-mediated apoptosis by mitogen-activated kinase signaling. J. Immunol. 160: 2626–2636.
   PubMedGoogle Scholar
• Holmstrüm, T. H., I. Schmitz, T. S. Süderstrüm, M. Poukkula, V. L. Johnson, S. C. Chow, P. H. Krammer, and J. E. Eriksson. 2000. MAPK/ERK signaling in activated T cells inhibits CD95/Fas-mediated apoptosis downstream of DISC assembly. EMBO J. 19: 5418–5428.
   PubMedGoogle Scholar
• Holmstrüm, T. H., S. E. F. Tran, V. L. Johnson, N. G. Ahn, S. C. Chow, and J. E. Eriksson. 1999. Inhibition of mitogen-activated kinase signaling sensitizes HeLa cells to Fas receptor-mediated apoptosis. Mol. Cell. Biol. 19: 5991–6002.
   PubMedGoogle Scholar
• Horita, M., E. J. Andreu, A. Benito, C. Arbona, C. Sanz, I. Benet, F. Prosper, and J. L. Fernandez-Luna. 2000. Blockade of the Bcr-Abl kinase activity induces apoptosis of chronic myelogenous leukemia cells by suppressing signal transducer and activator of transcription 5-dependent expression of Bcl-xL. J. Exp. Med. 191: 977–984.
   PubMed Web of Science ®Google Scholar
• Hu, S., C. Vincenz, J. Ni, R. Gentz, and V. M. Dixit. 1997. I-FLICE, a novel inhibitor of tumor necrosis factor receptor-1- and CD-95-induced apoptosis. J. Biol. Chem. 272: 17255–17257.
   PubMed Web of Science ®Google Scholar
• Inohara, N., T. Koseki, Y. Hu, S. Chen, and G. Nunez. 1997. CLARP, a death effector domain-containing protein interacts with caspase-8 and regulates apoptosis. Proc. Natl. Acad. Sci. USA 94: 10717–10722.
   PubMedGoogle Scholar
• Irmler, M., M. Thome, M. Hahne, P. Schneider, K. Hofmann, V. Steiner, J.-L. Bodmer, M. Schroter, K. Burns, C. Mattmann, D. Rimoldi, L. E. French, and J. Tschopp. 1997. Inhibition of death receptor signals by cellular FLIP. Nature 388: 190–195.
   PubMed Web of Science ®Google Scholar
• Itoh, N., S. Yonehara, A. Ishii, M. Yonehara, S. Mizushima, M. Sameshima, A. Hase, Y. Seto, and S. Nagata. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66: 233–243.
   PubMed Web of Science ®Google Scholar
• Jia, L., S. M. Kelsey, M. F. Grahn, X. R. Jiang, and A. C. Newland. 1996. Increased activity and sensitivity of mitochondrial respiratory enzymes to tumor necrosis factor alpha-mediated inhibition is associated with increased cytotoxicity in drug-resistant leukemic cell lines. Blood 87: 2401–2410.
   PubMed Web of Science ®Google Scholar
• Jia, L., S. M. Srinivasula, F. T. Liu, A. C. Newland, T. Fernandes-Alnemri, E. S. Alnemri, and S. M. Kelsey. 2001. Apaf-1 protein deficiency confers resistance to cytochrome c-dependent apoptosis in human leukemic cells. Blood 98: 414–421.
   PubMedGoogle Scholar
• Jo, M., T. H. Kim, D. W. Seol, J. E. Esplen, K. Dorko, T. R. Billiar, and S. C. Strom. 2000. Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat. Med. 6: 564–567.
   PubMed Web of Science ®Google Scholar
• Kataoka, T., R. C. Budd, N. Holler, M. Thome, F. Martinon, M. Irmler, K. Burns, M. Hahne, N. Kennedy, M. Kovacsovics, and J. Tschopp. 2000. The caspase-8 inhibitor FLIP promotes activation of NF-kappaB and Erk signaling pathways. Curr. Biol. 10: 640–648.
   PubMed Web of Science ®Google Scholar
• Keane, M. M., S. A. Ettenberg, M. M. Nau, E. K. Russell, and S. Lipkowitz. 1999. Chemotherapy augments TRAIL-induced apoptosis in breast cell lines. Cancer Res. 59: 734–741.
   PubMed Web of Science ®Google Scholar
• Kim, Y., N. Suh, M. Sporn, and J. C. Reed. 2002. An inducible pathway for degradation of FLIP protein sensitizes tumor cells to TRAIL-induced apoptosis. J. Biol. Chem. 277: 22320–22329.
   PubMed Web of Science ®Google Scholar
• Kirchhoff, S., W. W. Muller, A. Krueger, I. Schmitz, and P. H. Krammer. 2000. TCR-mediated up-regulation of c-FLIPshort correlates with resistance toward CD95-mediated apoptosis by blocking death-inducing signaling complex activity. J. Immunol. 165: 6293–6300.
   PubMedGoogle Scholar
• Kreuz, S., D. Siegmund, P. Scheurich, and H. Wajant. 2001. NF-κB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell. Biol. 21: 3964–3973.
   PubMed Web of Science ®Google Scholar
• Krueger, A., S. Baumann, P. H. Krammer, and S. Kirchhoff. 2001. FLICE-inhibitory proteins: regulators of death receptor-mediated apoptosis. Mol. Cell. Biol. 21: 8247–8254.
   PubMed Web of Science ®Google Scholar
• Krueger, A., I. Schmitz, S. Baumann, P. H. Krammer, and S. Kirchhoff. 2001. Cellular FLICE-inhibitory protein splice variants inhibit different steps of caspase-8 activation at the CD95 death-inducing signaling complex. J. Biol. Chem. 276: 20633–20640.
   PubMed Web of Science ®Google Scholar
• Landowski, T. H., K. H. Shain, M. M. Oshiro, I. Buyuksal, J. S. Painter, and W. S. Dalton. 1999. Myeloma cells selected for resistance to CD95-mediated apoptosis are not cross-resistant to cytotoxic drugs: evidence for independent mechanisms of caspase activation. Blood 94: 265–274.
   PubMed Web of Science ®Google Scholar
• Lawrence, D., Z. Shahrokh, S. Marsters, K. Achilles, D. Shih, B. Mounho, K. Hillan, K. Totpal, L. DeForge, P. Schow, J. Hooley, S. Sherwood, R. Pai, S. Leung, L. Khan, B. Gliniak, J. Bussiere, C. A. Smith, S. S. Strom, S. Kelley, J. A. Fox, D. Thomas, and A. Ashkenazi. 2001. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat. Med. 7: 383–385.
   PubMed Web of Science ®Google Scholar
• Leszczyniecka, M., T. Roberts, P. Dent, S. Grant, and P. B. Fisher. 2001. Differentiation therapy of human cancer: basic science and clinical applications. Pharmacol. Ther. 90: 105–156.
   PubMed Web of Science ®Google Scholar
• Lozzio, C. B., and B. B. Lozzio. 1975. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 45: 321–334.
   PubMed Web of Science ®Google Scholar
• Malik, Z., S. D. Chitayat, and Y. Langzam. 1988. Hemin dependent morphological maturation and endogenous porphyrin synthesis by K562 leukemic cells. Cancer Lett. 41: 203–209.
   PubMedGoogle Scholar
• Martin, P., and T. Papayannopoulou. 1982. HEL cells: a new human erythroleukemia cell line with spontaneous and induced globin expression. Science 216: 1233–1235.
   PubMed Web of Science ®Google Scholar
• McGahon, A., R. Bissonnette, M. Schmitt, K. M. Cotter, D. R. Green, and T. G. Cotter. 1994. BCR-ABL maintains resistance of chronic myelogenous leukemia cells to apoptotic cell death. Blood 83: 1179–1187.
   PubMed Web of Science ®Google Scholar
• Medema, J. P., J. de Jong, T. van Hall, C. J. Melief, and R. Offringa. 1999. Immune escape of tumors in vivo by expression of cellular FLICE-inhibitory protein. J. Exp. Med. 190: 1033–1038.
   PubMed Web of Science ®Google Scholar
• Micheau, O., S. Lens, O. Gaide, K. Alevizopoulos, and J. Tschopp. 2001. NF-κB signals induce the expression of c-FLIP. Mol. Cell. Biol. 21: 5299–5305.
   PubMed Web of Science ®Google Scholar
• Micheau, O., M. Thome, P. Schneider, N. Holler, J. Tschopp, D. W. Nicholson, C. Briand, and M. G. Grütter. 2002. The long form of FLIP is an activator of caspase-8 at the Fas death-inducing signaling complex. J. Biol. Chem. 277: 45162–45171.
   PubMedGoogle Scholar
• Nimmanapalli, R., M. Porosnicu, D. Nguyen, E. Worthington, E. O'Bryan, C. Perkins, and K. Bhalla. 2001. Cotreatment with STI-571 enhances tumor necrosis factor alpha-related apoptosis-inducing ligand (TRAIL or apo-2L)-induced apoptosis of Bcr-Abl-positive human acute leukemia cells. Clin. Cancer Res. 7: 350–357.
   PubMed Web of Science ®Google Scholar
• Pan, G., J. Ni, Y. F. Wei, G. Yu, R. Gentz, and V. M. Dixit. 1997. An antagonist decoy receptor and a death domain-containing receptor for TRAIL. Science 277: 815–818.
   PubMed Web of Science ®Google Scholar
• Pan, G., K. O'Rourke, A. M. Chinnaiyan, R. Gentz, R. Ebner, J. Ni, and V. M. Dixit. 1997. The receptor for the cytotoxic ligand TRAIL. Science 276: 111–113.
   PubMed Web of Science ®Google Scholar
• Pitti, R. M., S. A. Marsters, S. Ruppert, C. J. Donahue, A. Moore, and A. Ashkenazi. 1996. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271: 12687–12690.
   PubMed Web of Science ®Google Scholar
• Plasilova, M., J. Zivny, J. Jelinek, R. Neuwirtova, J. Cermak, E. Necas, L. Andera, and T. Stopka. 2002. TRAIL (Apo2L) suppresses growth of primary human leukemia and myelodysplasia progenitors. Leukemia 16: 67–73.
   PubMed Web of Science ®Google Scholar
• Rasper, D. M., J. P. Vaillancourt, S. Hadano, V. M. Houtzager, I. Seiden, S. L. Keen, P. Tawa, S. Xanthoudakis, J. Nasir, D. Martindale, B. F. Koop, E. P. Peterson, N. A. Thornberry, J. Huang, D. P. MacPherson, S. C. Black, F. Hornung, M. J. Lenardo, M. R. Hayden, S. Roy, and D. W. Nicholson. 1998. Cell death attenuation by ′Usurpin', a mammalian DED-caspase homologue that precludes caspase-8 recruitment and activation by the CD-95 (Fas, APO-1) receptor complex. Cell Death Differ. 5: 271–288.
   PubMed Web of Science ®Google Scholar
• Scaffidi, C., I. Schmitz, P. H. Krammer, and M. E. Peter. 1999. The role of c-FLIP in modulation of CD95-induced apoptosis. J. Biol. Chem. 274: 1541–1548.
   PubMed Web of Science ®Google Scholar
• Sheridan, J. P., S. A. Marsters, R. M. Pitti, A. Gurney, M. Skubatch, D. Baldwin, L. Ramakrishnan, C. L. Gray, K. Baker, W. I. Wood, A. D. Goddard, P. Godowski, and A. Ashkenazi. 1997. Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277: 818–821.
   PubMed Web of Science ®Google Scholar
• Shu, H.-B., D. R. Halpin, and D. V. Goeddel. 1997. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity 6: 751–763.
   PubMed Web of Science ®Google Scholar
• Srinivasula, S. M., M. Ahmad, S. Ottilie, F. Bullrich, S. Banks, Y. Wang, T. Fernandes-Alnemri, C. M. Croce, G. Litwack, K. J. Tomaselli, R. C. Armstrong, and E. S. Alnemri. 1997. FLAME-1, a novel FADD-like anti-apoptotic molecule that regulates Fas/TNFR1-induced apoptosis. J. Biol. Chem. 272: 18542–18545.
   PubMed Web of Science ®Google Scholar
• Strasser, A., L. O'Connor, and V. M. Dixit. 2000. Apoptosis signaling. Annu. Rev. Biochem. 69: 217–245.
   PubMed Web of Science ®Google Scholar
• Terui, Y., Y. Furukawa, J. Kikuchi, S. Iwase, K. Hatake, and Y. Miura. 1998. Bcl-x is a regulatory factor of apoptosis and differentiation in megakaryocytic lineage cells. Exp. Hematol. 26: 236–244.
   PubMedGoogle Scholar
• Thome, M., P. Schneider, K. Hofmann, H. Fickenscher, E. Meinl, F. Neipel, C. Mattmann, K. Burns, J. L. Bodmer, M. Schroter, C. Scaffidi, P. H. Krammer, M. E. Peter, and J. Tschopp. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386: 517–521.
   PubMed Web of Science ®Google Scholar
• Tran, S. E., T. H. Holmstrüm, M. Ahonen, V.-M. Kähäri, and J. E. Eriksson. 2001. MAPK/ERK overrides the apoptotic signaling from Fas, TNF, and TRAIL receptors. J. Biol. Chem. 276: 16484–16490.
   PubMedGoogle Scholar
• Vondracek, J., M. A. Sheard, P. Krejci, K. Minksova, J. Hofmanova, and A. Kozubik. 2001. Modulation of death receptor-mediated apoptosis in differentiating human myeloid leukemia HL-60 cells. J. Leukoc. Biol. 69: 794–802.
   PubMed Web of Science ®Google Scholar
• Walczak, H., A. Bouchon, H. Stahl, and P. H. Krammer. 2000. Tumor necrosis factor-related apoptosis-inducing ligand retains its apoptosis-inducing capacity on Bcl-2- or Bcl-xL-overexpressing chemotherapy-resistant tumor cells. Cancer Res. 60: 3051–3057.
   PubMed Web of Science ®Google Scholar
• Walczak, H., R. E. Miller, K. Ariail, B. Gliniak, T. S. Griffith, M. Kubin, W. Chin, J. Jones, A. Woodward, T. Le, C. Smith, P. Smolak, R. G. Goodwin, C. T. Rauch, J. C. Schuh, and D. H. Lynch. 1999. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat. Med. 5: 157–163.
   PubMed Web of Science ®Google Scholar
• Wallach, D., A. V. Kovalenko, E. E. Varfolomeev, and M. P. Boldin. 1998. Death-inducing functions of ligands of the tumor necrosis factor family: a Sanhedrin verdict. Curr. Opin. Immunol. 10: 279–288.
   PubMedGoogle Scholar
• Wiley, S. R., K. Schooley, P. J. Smolak, W. S. Din, C. P. Huang, J. K. Nicholl, G. R. Sutherland, T. D. Smith, C. Rauch, and C. A. Smith. 1995. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3: 673–682.
   PubMed Web of Science ®Google Scholar
• Yeh, W. C., A. Itie, A. J. Elia, M. Ng, H. B. Shu, A. Wakeham, C. Mirtsos, N. Suzuki, M. Bonnard, D. V. Goeddel, and T. W. Mak. 2000. Requirement for Casper (c-FLIP) in regulation of death receptor-induced apoptosis and embryonic development. Immunity 12: 633–642.
   PubMed Web of Science ®Google Scholar
• Zamai, L., P. Secchiero, S. Pierpaoli, A. Bassini, S. Papa, E. S. Alnemri, L. Guidotti, M. Vitale, and G. Zauli. 2000. TNF-related apoptosis-inducing ligand (TRAIL) as a negative regulator of normal human erythropoiesis. Blood 95: 3716–3724.
   PubMed Web of Science ®Google Scholar
• Zang, D. Y., R. G. Goodwin, M. R. Loken, E. Bryant, and H. J. Deeg. 2001. Expression of tumor necrosis factor-related apoptosis-inducing ligand, Apo2L, and its receptors in myelodysplastic syndrome: effects on in vitro hemopoiesis. Blood 98: 3058–3065.
   PubMed Web of Science ®Google Scholar